Neuronal activity maps (bottom) in the striatum as animals make different movements (top). Credit: Andreas Klaus and Gabriela Martins

At any moment in time, our brains can choose among a number of possible actions. Sitting at your desk, you might get up to grab a cup of coffee, start writing an email, check Facebook or scratch your nose. How does the brain decide which option takes precedence? A region called the basal ganglia is essential for making these decisions. But scientists don’t yet know how the choice is made.

New research from Rui Costa, a neuroscientist at Columbia University, and collaborators takes a step in answering that question. They showed that groups of neurons in a specific part of the basal ganglia, the striatum, represent different movements. Now that researchers have an idea of how different options are represented, they can start to look at where and how these options emerge and how they are selected.

Costa’s group had shown back in 2004 that certain neurons in the striatum represent the speed of a movement — if an animal performed a movement quickly, one such neuron might be highly active, but much less active if the animal performed the same movement slowly. In a 2014 study, Costa and collaborators showed that the striatal neurons had activity related to what the animal was doing and these neurons were modulated by the speed of movement.

These findings suggested that the striatum should also have neurons that represent just the action, regardless of the speed the action is performed. A tennis player, for example, can execute a lightning-fast serve in a match or a gentle serve when instructing a novice. “Is there an abstract representation of the action that’s independent of speed?” Costa asks.

The researchers used a microendoscope, a miniature microscope implanted in the brain, to simultaneously track activity of hundreds of neurons in the striatum as mice moved freely in an open field. A series of sensors, including gyroscopes and accelerometers, tracked the animals’ movements, and a specialized algorithm automatically classified those behaviors.

A two dimensional plot of the animal's movement clusters into distinct behaviors. Credit: Andreas Klaus and Gabriela Martins

Comparing behavior and neural activity, the researchers found that the striatum does indeed possess a representation of the animal’s movements. “The activity of particular neurons was very related to the execution of a particular action,” Costa says. The representations seem to be relatively stable across the speeds at which the animal performs the action. The research was published in Neuron in August.

The researchers found that neuronal representations for more similar actions were more closely related, with more neurons in common, than were representations of more distinct actions; neuronal representations for very different actions had very little overlap. Costa theorizes this type of representation could guide behavior in novel situations. “A continuum of action space represented in an abstract manner might help you select an action from the abstract action space, even when you don’t know which particular action is the best option,” Costa says. If turning to the left is a bad choice in a particular situation, automatically being able to choose a very different action, without having tried it before, could be helpful.

Neuronal activity of spiny projection neurons of the striatum as animals walk around an open field. Credit: Andreas Klaus and Gabriela Martins

Costa notes that the striatal map may represent more than just a muscle map or a somatosensory map. Movements that use similar muscles but are behaviorally distinct, such as turning the head to the left or right, have very different striatal representations. In a muscle map, these two movements would have similar representations.

However, interpreting exactly what the map represents can be a challenge. Costa’s team studied freely moving animals, which may be difficult to decipher. “This is spontaneous self-generated behavior, and we don’t know the inputs driving it,” says Peter Redgrave, a neuroscientist at the University of Sheffield. In an open-field environment, mice tend to run along the edge of the box, using their whiskers to guide them. “How much of the brain activity they report is associated with the selection of locomotor movements, rather than the consequence of somatosensory input from the whisker?” Redgrave says. “Whether the basal ganglia is selecting the sensory input that is being permitted to guide movement — head turn left — or the movement itself — head turn left — is still very much an open question.” Both options could generate the same activity patterns, he says.

Costa and collaborators are now looking at how these representations are formed and how they are used to select movement. The motor cortex is one of the major inputs to the basal ganglia, and previous research suggests that it houses representations of different possible actions. Costa wants to figure out whether all of these options are sent to the basal ganglia, which then chooses among them. Or if the selection takes place in the motor cortex, and the basal ganglia then decides whether to execute that action.

To answer this question, his team is recording from the basal ganglia in animals trained to choose among one of three possible actions. The researchers will examine how each option is represented in the basal ganglia, as well as how that options emerges. Does it pop up suddenly? Or do multiple options exist briefly before one wins out? They are also developing methods to record from both the motor cortex and basal ganglia to study how information is transmitted from one region to another.

The researchers plan to look at what happens to these representations in movement disorders, such as Parkinson’s disease, where people have difficulty initiating movement, and conditions with repetitive behavior, such as obsessive-compulsive disorder and autism.